Epigallocatechin-3-gallate upregulates miR-221 to inhibit osteopontin-dependent hepatic fibrosis

PLoS ONE

Volumn 11, Issue 12, 2016, Pages

  Arffa, M L ^a   Zapf, M A ^a   Kothari, A N ^a   Chang, V ^a   Gupta, G N ^a   Ding, X ^a   Al Gayyar, M M ^b,e   Syn, W ^c,d   Elsherbiny, N M ^b   Kuo, P C ^a   Mi, Z ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b MANSOURA UNIVERSITY   (Egypt)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^e UNIVERSITY OF TABUK   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

EPIGALLOCATECHIN GALLATE; MICRORNA; MICRORNA 10B; MICRORNA 181A; MICRORNA 221; OSTEOPONTIN; THIOACETAMIDE; UNCLASSIFIED DRUG; ANTIOXIDANT; CATECHIN; MIRN221 MICRORNA, RAT; TEA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; GENE EXPRESSION REGULATION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; LIVER FIBROSIS; LIVER INJURY; MALE; NONHUMAN; OPN GENE; RAT; RNA DEGRADATION; STELLATE CELL; UPREGULATION; WOUND CLOSURE; ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENETICS; HEP-G2 CELL LINE; HEPATIC STELLATE CELL; HUMAN; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; TEA;

ANIMALS; ANTIOXIDANTS; CATECHIN; CELL LINE; HEP G2 CELLS; HEPATIC STELLATE CELLS; HUMANS; LIVER CIRRHOSIS; MALE; MICRORNAS; OSTEOPONTIN; RATS, SPRAGUE-DAWLEY; TEA; UP-REGULATION;

EID: 85006001499     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0167435     Document Type: Article

References (57)

1. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005 Feb 1; 115(2):209-218. doi: 10.1172/JCI24282 PMID: 15690074
2. Lim YS, Kim WR. The global impact of hepatic fibrosis and end-stage liver disease. Clin Liver Dis 2008 Nov; 12(4):733-46, vii. doi: 10.1016/j.cld.2008.07.007 PMID: 18984463
3. Gines P, Cardenas A, Arroyo V, Rodes J. Management of cirrhosis and ascites. N Engl J Med 2004 Apr 15; 350(16):1646-1654. doi: 10.1056/NEJMra035021 PMID: 15084697
4. Coombes JD, Choi SS, Swiderska-Syn M, Manka PP, Reid D, Palma E, et al. Osteopontin is a proximal effector of leptin-mediated non-alcoholic steatohepatitis (NASH) fibrosis. Biochim Biophys Acta 2015 Oct 31.
5. Coombes JD, Swiderska-Syn M, Dolle L, Reid D, Eksteen B, Claridge L, et al. Osteopontin neutralisation abrogates the liver progenitor cell response and fibrogenesis in mice. Gut 2015 Jul; 64(7):1120-1131. doi: 10.1136/gutjnl-2013-306484 PMID: 24902765
6. Tan TK, Zheng G, Hsu TT, Lee SR, Zhang J, Zhao Y, et al. Matrix metalloproteinase-9 of tubular and macrophage origin contributes to the pathogenesis of renal fibrosis via macrophage recruitment through osteopontin cleavage. Lab Invest 2013 Apr; 93(4):434-449. doi: 10.1038/labinvest.2013.3 PMID: 23358111
7. Oh K, Seo MW, Kim YW, Lee DS. Osteopontin Potentiates Pulmonary Inflammation and Fibrosis by Modulating IL-17/IFN-Î-secreting T-cell Ratios in Bleomycin-treated Mice. Immune Netw 2015 Jun; 15 (3):142-149. doi: 10.4110/in.2015.15.3.142 PMID: 26140046
8. Simao A, Madaleno J, Silva N, Rodrigues F, Caseiro P, Costa JN, et al. Plasma osteopontin is a biomarker for the severity of alcoholic liver cirrhosis, not for hepatocellular carcinoma screening. BMC Gastroenterol 2015 Jun 30; 15:73-015-0307-1.
9. Matsue Y, Tsutsumi M, Hayashi N, Saito T, Tsuchishima M, Toshikuni N, et al. Serum osteopontin predicts degree of hepatic fibrosis and serves as a biomarker in patients with hepatitis C virus infection. PLoS One 2015 Mar 11; 10(3):e0118744. doi: 10.1371/journal.pone.0118744 PMID: 25760884
10. Patouraux S, Bonnafous S, Voican CS, Anty R, Saint-Paul MC, Rosenthal-Allieri MA, et al. The osteopontin level in liver, adipose tissue and serum is correlated with fibrosis in patients with alcoholic liver disease. PLoS One 2012; 7(4):e35612. doi: 10.1371/journal.pone.0035612 PMID: 22530059
11. Huang W, Zhu G, Huang M, Lou G, Liu Y, Wang S. Plasma osteopontin concentration correlates with the severity of hepatic fibrosis and inflammation in HCV-infected subjects. Clin Chim Acta 2010 May 2; 411(9-10):675-678. doi: 10.1016/j.cca.2010.01.029 PMID: 20138033
12. Arriazu E, Ge X, Leung TM, Magdaleno F, Lopategi A, Lu Y, et al. Signalling via the osteopontin and high mobility group box-1 axis drives the fibrogenic response to liver injury. Gut 2016 Jan 27.
13. Sahai A, Malladi P, Melin-Aldana H, Green RM, Whitington PF. Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am J Physiol Gastrointest Liver Physiol 2004 Jul; 287(1):G264-73. doi: 10.1152/ajpgi.00002.2004 PMID: 15044174
14. Strazzabosco M, Fabris L, Albano E. Osteopontin: a new player in regulating hepatic ductular reaction and hepatic progenitor cell responses during chronic liver injury. Gut 2014 Nov; 63(11):1693-1694. doi: 10.1136/gutjnl-2014-307712 PMID: 25056656
15. Leung TM, Wang X, Kitamura N, Fiel MI, Nieto N. Osteopontin delays resolution of liver fibrosis. Lab Invest 2013 Oct; 93(10):1082-1089. doi: 10.1038/labinvest.2013.104 PMID: 23999249
16. Kim HK, Yang TH, Cho HY. Antifibrotic effects of green tea on in vitro and in vivo models of liver fibrosis. World J Gastroenterol 2009 Nov 7; 15(41):5200-5205. doi: 10.3748/wjg.15.5200 PMID: 19891020
17. Suzuki Y., Miyoshi N., & Isemura M. Health-promoting effects of green tea. Proc Jpn Acad Ser B Phys Biol Sci 2012 Mar 9; 88(3):88-101. doi: 10.2183/pjab.88.88 PMID: 22450537
18. Ui A, Kuriyama S, Kakizaki M, Sone T, Nakaya N, Ohmori-Matsuda K, et al. Green tea consumption and the risk of liver cancer in Japan: the Ohsaki Cohort study. Cancer Causes Control 2009 Dec; 20 (10):1939-1945. doi: 10.1007/s10552-009-9388-x PMID: 19768563
19. Yin X, Yang J, Li T, Song L, Han T, Yang M, et al. The effect of green tea intake on risk of liver disease: a meta analysis. Int J Clin Exp Med 2015; 8(6):8339-8346. PMID: 26309486
20. Yuan JM. Cancer prevention by green tea: evidence from epidemiologic studies. Am J Clin Nutr 2013 Dec; 98(6 Suppl):1676S-1681S. doi: 10.3945/ajcn.113.058271 PMID: 24172305
21. Zhong Z, Froh M, Lehnert M, Schoonhoven R, Yang L, Lind H, et al. Polyphenols from Camellia sinenesis attenuate experimental cholestasis-induced liver fibrosis in rats. Am J Physiol Gastrointest Liver Physiol 2003 Nov; 285(5):G1004-13. doi: 10.1152/ajpgi.00008.2003 PMID: 12791596
22. Ding Y, Sun X, Chen Y, Deng Y, Qian K. Epigallocatechin gallate attenuated non-alcoholic steatohepatitis induced by methionine- and choline-deficient diet. Eur J Pharmacol 2015 Aug 15; 761:405-412. doi: 10.1016/j.ejphar.2015.05.005 PMID: 25967348
23. Santamarina AB, Carvalho-Silva M, Gomes LM, Okuda MH, Santana AA, Streck EL, et al. Decaffeinated green tea extract rich in epigallocatechin-3-gallate prevents fatty liver disease by increased activities of mitochondrial respiratory chain complexes in diet-induced obesity mice. J Nutr Biochem 2015 Nov; 26(11):1348-1356. doi: 10.1016/j.jnutbio.2015.07.002 PMID: 26300331
24. Sriram N, Kalayarasan S, Manikandan R, Arumugam M, Sudhandiran G. Epigallocatechin gallate attenuates fibroblast proliferation and excessive collagen production by effectively intervening TGF-beta1 signalling. Clin Exp Pharmacol Physiol 2015 Aug; 42(8):849-859. doi: 10.1111/1440-1681.12428 PMID: 26010495
25. Zapf MA, Kothari AN, Weber CE, Arffa ML, Wai PY, Driver J, et al. Green tea component epigallocatechin-3-gallate decreases expression of osteopontin via a decrease in mRNA half-life in cell lines of metastatic hepatocellular carcinoma. Surgery 2015 Oct; 158(4):1039-1048. doi: 10.1016/j.surg.2015.06. 011 PMID: 26189955
26. Bhattacharya SD, Garrison J, Guo H, Mi Z, Markovic J, Kim VM, et al. Micro-RNA-181a regulates osteopontin-dependent metastatic function in hepatocellular cancer cell lines. Surgery 2010 Aug; 148 (2):291-297. doi: 10.1016/j.surg.2010.05.007 PMID: 20576283
27. Tsang WP, Kwok TT. Epigallocatechin gallate up-regulation of miR-16 and induction of apoptosis in human cancer cells. J Nutr Biochem 2010 Feb; 21(2):140-146. doi: 10.1016/j.jnutbio.2008.12.003 PMID: 19269153
28. Ahn J, Jeong KJ, Ko M, Shin HJ, Kim HS, Chung HJ, et al. Changes of miRNA and mRNA expression in HepG2 cells treated by epigallocatechin gallate. Molecular & Cellular Toxicology 2010; 6(2):169-177.
29. Arola-Arnal A, Blade C. Proanthocyanidins modulate microRNA expression in human HepG2 cells. PLoS One 2011; 6(10):e25982. doi: 10.1371/journal.pone.0025982 PMID: 21998738
30. Milenkovic D, Deval C, Gouranton E, Landrier JF, Scalbert A, Morand C, et al. Modulation of miRNA expression by dietary polyphenols in apoE deficient mice: a new mechanism of the action of polyphenols. PLoS One 2012; 7(1):e29837. doi: 10.1371/journal.pone.0029837 PMID: 22253797
31. Yamada S, Tsukamoto S, Huang Y, Makio A, Kumazoe M, Yamashita S, et al. Epigallocatechin-3-Ogallate up-regulates microRNA-let-7b expression by activating 67-kDa laminin receptor signaling in melanoma cells. Sci Rep 2016 Jan 12; 6:19225. doi: 10.1038/srep19225 PMID: 26754091
32. Mi Z, Guo H, Russell MB, Liu Y, Sullenger BA, Kuo PC. RNA Aptamer Blockade of Osteopontin Inhibits Growth and Metastasis of MDA-MB231 Breast Cancer Cells. Mol Ther 2009 Jan; 17(1):153-161. doi: 10.1038/mt.2008.235 PMID: 18985031
33. Torres AG, Fabani MM, Vigorito E, Gait MJ. MicroRNA fate upon targeting with anti-miRNA oligonucleotides as revealed by an improved Northern-blot-based method for miRNA detection. RNA 2011 May; 17 (5):933-943. doi: 10.1261/rna.2533811 PMID: 21441346
34. Tian RQ, Wang XH, Hou LJ, Jia WH, Yang Q, Li YX, et al. MicroRNA-372 Is Down-regulated and Targets Cyclin-dependent Kinase 2 (CDK2) and Cyclin A1 in Human Cervical Cancer, Which May Contribute to Tumorigenesis. J Biol Chem 2011 Jul 22; 286(29):25556-25563. doi: 10.1074/jbc.M111.221564 PMID: 21646351
35. Darweish MM, Abbas A, Ebrahim MA, Al-Gayyar MM. Chemopreventive and hepatoprotective effects of Epigallocatechin-gallate against hepatocellular carcinoma: role of heparan sulfate proteoglycans pathway. J Pharm Pharmacol 2014 Jul; 66(7):1032-1045. doi: 10.1111/jphp.12229 PMID: 24611903
36. Wang X, Lopategi A, Ge X, Lu Y, Kitamura N, Urtasun R, et al. Osteopontin induces ductular reaction contributing to liver fibrosis. Gut 2014 Nov; 63(11):1805-1818. doi: 10.1136/gutjnl-2013-306373 PMID: 24496779
37. Ullmann U, Haller J, Decourt J, Girault N, Girault J, Richard-Caudron A, et al. A Single Ascending Dose Study of Epigallocatechin Gallate in Healthy Volunteers. Journal of International Medical Research 2003 April 01; 31(2):88-101. PMID: 12760312
38. Chow HS, Hakim IA, Vining DR, Crowell JA, Ranger-Moore J, Chew WM, et al. Effects of Dosing Condition on the Oral Bioavailability of Green Tea Catechins after Single-Dose Administration of Polyphenon E in Healthy Individuals. Clinical Cancer Research 2005 June 15; 11(12):4627-4633. doi: 10.1158/1078-0432.CCR-04-2549 PMID: 15958649
39. Sodek J, Ganss B, McKee MD. Osteopontin. Crit Rev Oral Biol Med 2000; 11(3):279-303. PMID: 11021631
40. Zheng C, Yinghao S, Li J. MiR-221 expression affects invasion potential of human prostate carcinoma cell lines by targeting DVL2. Med Oncol 2012 Jun; 29(2):815-822. doi: 10.1007/s12032-011-9934-8 PMID: 21487968
41. Koelz M, Lense J, Wrba F, Scheffler M, Dienes HP, Odenthal M. Down-regulation of miR-221 and miR-222 correlates with pronounced Kit expression in gastrointestinal stromal tumors. Int J Oncol 2011 Feb; 38(2):503-511. doi: 10.3892/ijo.2010.857 PMID: 21132270
42. Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F, et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci U S A 2005 Dec 13; 102(50):18081-18086. doi: 10.1073/pnas.0506216102 PMID: 16330772
43. John K, Hadem J, Krech T, Wahl K, Manns MP, Dooley S, et al. MicroRNAs play a role in spontaneous recovery from acute liver failure. Hepatology 2014 Oct; 60(4):1346-1355. doi: 10.1002/hep.27250 PMID: 24913549
44. Sharma AD, Narain N, Handel EM, Iken M, Singhal N, Cathomen T, et al. MicroRNA-221 regulates FAS-induced fulminant liver failure. Hepatology 2011 May; 53(5):1651-1661. doi: 10.1002/hep.24243 PMID: 21400558
45. Yuan Q, Loya K, Rani B, Mobus S, Balakrishnan A, Lamle J, et al. MicroRNA-221 overexpression accelerates hepatocyte proliferation during liver regeneration. Hepatology 2013 Jan; 57(1):299-310. doi: 10.1002/hep.25984 PMID: 22821679
46. Yang J, Han S, Huang W, Chen T, Liu Y, Pan S, et al. A Meta-Analysis of MicroRNA Expression in Liver Cancer. PLoS One 2014; 9(12):e114533. doi: 10.1371/journal.pone.0114533 PMID: 25490558
47. Callegari E, Elamin BK, Giannone F, Milazzo M, Altavilla G, Fornari F, et al. Liver tumorigenicity promoted by microRNA-221 in a mouse transgenic model. Hepatology 2012 Sep; 56(3):1025-1033. doi: 10.1002/hep.25747 PMID: 22473819
48. Broderick JA, Zamore PD. MicroRNA therapeutics. Gene Ther 2011 Dec; 18(12):1104-1110. doi: 10.1038/gt.2011.50 PMID: 21525952
49. Kota J., Chivukula R. R., O'Donnell K. A., Wentzel E. A., Montgomery C. L., Hwang H. W, et al. Therapeutic delivery of miR-26a inhibits cancer cell proliferation and induces tumor-specific apoptosis. Cell 2009 Jun 12; 137(6):1005-1017. doi: 10.1016/j.cell.2009.04.021 PMID: 19524505
50. Safer AM, Afzal M, Hanafy N, Mousa S. Green tea extract therapy diminishes hepatic fibrosis mediated by dual exposure to carbon tetrachloride and ethanol: A histopathological study. Exp Ther Med 2015 Mar; 9(3):787-794. doi: 10.3892/etm.2014.2158 PMID: 25667629
51. Xiao J, Ho CT, Liong EC, Nanji AA, Leung TM, Lau TY, et al. Epigallocatechin gallate attenuates fibrosis, oxidative stress, and inflammation in non-alcoholic fatty liver disease rat model through TGF/SMAD, PI3 K/Akt/FoxO1, and NF-kappa B pathways. Eur J Nutr 2014 Feb; 53(1):187-199. doi: 10.1007/s00394-013-0516-8 PMID: 23515587
52. Hung GD, Li PC, Lee HS, Chang HM, Chien CT, Lee KL. Green tea extract supplementation ameliorates CCl4-induced hepatic oxidative stress, fibrosis, and acute-phase protein expression in rat. J Formos Med Assoc 2012 Oct; 111(10):550-559. doi: 10.1016/j.jfma.2011.06.026 PMID: 23089690
53. Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol 2011 Dec 15; 82(12):1807-1821. doi: 10.1016/j.bcp.2011.07.093 PMID: 21827739
54. Shen CJ, Tsou YA, Chen HL, Huang HJ, Wu SC, Cheng WTK, et al. Osteoponin Promoter Controlled by DNA Methylation: Aberrant Methylation in Cloned Porcine Genome. Biomed Res Int 2014; 2014.
55. Kuzuhara T, Tanabe A, Sei Y, Yamaguchi K, Suganuma M, Fujiki H. Synergistic effects of multiple treatments, and both DNA and RNA direct bindings on, green tea catechins. Mol Carcinog 2007 Aug; 46 (8):640-645. doi: 10.1002/mc.20332 PMID: 17440927
56. Kuzuhara T, Sei Y, Yamaguchi K, Suganuma M, Fujiki H. DNA and RNA as new binding targets of green tea catechins. J Biol Chem 2006 Jun 23; 281(25):17446-17456. doi: 10.1074/jbc.M601196200 PMID: 16641087
57. Baselga-Escudero L, Blade C, Ribas-Latre A, Casanova E, SuÁrez M, Torres JL, et al. Resveratrol and EGCG bind directly and distinctively to miR-33a and miR-122 and modulate divergently their levels in hepatic cells. Nucleic Acids Res 2014 Jan; 42(2):882-892 doi: 10.1093/nar/gkt1011 PMID: 24165878